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Title: Molecular basis for enantioselective herbicide degradation imparted by aryloxyalkanoate dioxygenases in transgenic plants

Abstract

The synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D) is an active ingredient of thousands of commercial herbicides. Multiple species of bacteria degrade 2,4-D via a pathway initiated by the Fe(II) and α-ketoglutarate (Fe/αKG)-dependent aryloxyalkanoate dioxygenases (AADs). Recently, genes encoding 2 AADs have been deployed commercially in herbicide-tolerant crops. Some AADs can also inactivate chiral phenoxypropionate and aryloxyphenoxypropionate (AOPP) herbicides, albeit with varying substrate enantioselectivities. Certain AAD enzymes, such as AAD-1, have expanded utility in weed control systems by enabling the use of diverse modes of action with a single trait. Here, we report 1) the use of a genomic context-based approach to identify 59 additional members of the AAD class, 2) the biochemical characterization of AAD-2 from Bradyrhizobium diazoefficiens USDA 110 as a catalyst to degrade (S)-stereoisomers of chiral synthetic auxins and AOPP herbicides, 3) spectroscopic data that demonstrate the canonical ferryl complex in the AAD-1 reaction, and 4) crystal structures of representatives of the AAD class. Structures of AAD-1, an (R)-enantiomer substrate-specific enzyme, in complexes with a phenoxypropionate synthetic auxin or with AOPP herbicides and of AAD-2, which has the opposite (S)-enantiomeric substrate specificity, reveal the structural basis for stereoselectivity and provide insights into a common catalytic mechanism.

Authors:
 [1];  [1]; ORCiD logo [2];  [3];  [3]; ORCiD logo [3]; ORCiD logo [3];  [2];  [1]
  1. Univ. of Illinois at Urbana-Champaign, IL (United States)
  2. Corteva Agriscience, Indianapolis, IN (United States)
  3. Pennsylvania State Univ., University Park, PA (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE
OSTI Identifier:
1544884
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
[ Journal Volume: 116; Journal Issue: 27]; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; herbicide; auxin; enzyme; resistance; mechanism

Citation Formats

Chekan, Jonathan R., Ongpipattanakul, Chayanid, Wright, Terry R., Zhang, Bo, Bollinger, J. Martin, Rajakovich, Lauren J., Krebs, Carsten, Cicchillo, Robert M., and Nair, Satish K. Molecular basis for enantioselective herbicide degradation imparted by aryloxyalkanoate dioxygenases in transgenic plants. United States: N. p., 2019. Web. doi:10.1073/pnas.1900711116.
Chekan, Jonathan R., Ongpipattanakul, Chayanid, Wright, Terry R., Zhang, Bo, Bollinger, J. Martin, Rajakovich, Lauren J., Krebs, Carsten, Cicchillo, Robert M., & Nair, Satish K. Molecular basis for enantioselective herbicide degradation imparted by aryloxyalkanoate dioxygenases in transgenic plants. United States. doi:10.1073/pnas.1900711116.
Chekan, Jonathan R., Ongpipattanakul, Chayanid, Wright, Terry R., Zhang, Bo, Bollinger, J. Martin, Rajakovich, Lauren J., Krebs, Carsten, Cicchillo, Robert M., and Nair, Satish K. Mon . "Molecular basis for enantioselective herbicide degradation imparted by aryloxyalkanoate dioxygenases in transgenic plants". United States. doi:10.1073/pnas.1900711116.
@article{osti_1544884,
title = {Molecular basis for enantioselective herbicide degradation imparted by aryloxyalkanoate dioxygenases in transgenic plants},
author = {Chekan, Jonathan R. and Ongpipattanakul, Chayanid and Wright, Terry R. and Zhang, Bo and Bollinger, J. Martin and Rajakovich, Lauren J. and Krebs, Carsten and Cicchillo, Robert M. and Nair, Satish K.},
abstractNote = {The synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D) is an active ingredient of thousands of commercial herbicides. Multiple species of bacteria degrade 2,4-D via a pathway initiated by the Fe(II) and α-ketoglutarate (Fe/αKG)-dependent aryloxyalkanoate dioxygenases (AADs). Recently, genes encoding 2 AADs have been deployed commercially in herbicide-tolerant crops. Some AADs can also inactivate chiral phenoxypropionate and aryloxyphenoxypropionate (AOPP) herbicides, albeit with varying substrate enantioselectivities. Certain AAD enzymes, such as AAD-1, have expanded utility in weed control systems by enabling the use of diverse modes of action with a single trait. Here, we report 1) the use of a genomic context-based approach to identify 59 additional members of the AAD class, 2) the biochemical characterization of AAD-2 from Bradyrhizobium diazoefficiens USDA 110 as a catalyst to degrade (S)-stereoisomers of chiral synthetic auxins and AOPP herbicides, 3) spectroscopic data that demonstrate the canonical ferryl complex in the AAD-1 reaction, and 4) crystal structures of representatives of the AAD class. Structures of AAD-1, an (R)-enantiomer substrate-specific enzyme, in complexes with a phenoxypropionate synthetic auxin or with AOPP herbicides and of AAD-2, which has the opposite (S)-enantiomeric substrate specificity, reveal the structural basis for stereoselectivity and provide insights into a common catalytic mechanism.},
doi = {10.1073/pnas.1900711116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = [27],
volume = [116],
place = {United States},
year = {2019},
month = {6}
}

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    Works referencing / citing this record:

    Transgenic Tobacco Plants Expressing a Bacterial Detoxifying Enzyme are Resistant to 2,4-D
    journal, August 1989

    • Streber, Wolfgang R.; Willmitzer, Lothar
    • Nature Biotechnology, Vol. 7, Issue 8
    • DOI: 10.1038/nbt0889-811

    Inhibition of Acetyl-CoA Carboxylase Activity by Haloxyfop and Tralkoxydim
    journal, January 1988


    The 2, 4-dichlorophenol hydroxylase of Alcaligenes eutrophus JMP134 is a homotetramer
    journal, February 1997

    • Farhana, Lulu; New, Peter B.
    • Canadian Journal of Microbiology, Vol. 43, Issue 2
    • DOI: 10.1139/m97-027

    Auxin molecular field maps define AUX1 selectivity: many auxin herbicides are not substrates
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    • Hoyerova, Klara; Hosek, Petr; Quareshy, Mussa
    • New Phytologist, Vol. 217, Issue 4
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    Resistance of Enlist (AAD-12) Cotton to Glufosinate
    journal, June 2017

    • Braxton, L. Bo; Richburg, John S.; York, Alan C.
    • Weed Technology, Vol. 31, Issue 3
    • DOI: 10.1017/wet.2017.14

    Vanadyl as a Stable Structural Mimic of Reactive Ferryl Intermediates in Mononuclear Nonheme-Iron Enzymes
    journal, September 2017


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    • DOI: 10.1021/ar700066p

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    • Journal of the American Chemical Society, Vol. 139, Issue 39
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    A cheminformatics review of auxins as herbicides
    journal, September 2017

    • Quareshy, Mussa; Prusinska, Justyna; Li, Jun
    • Journal of Experimental Botany, Vol. 69, Issue 2
    • DOI: 10.1093/jxb/erx258

    Insight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicide: 2,4-D works as herbicide
    journal, January 2014

    • Song, Yaling
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    • DOI: 10.1111/jipb.12131

    From perception to attenuation: auxin signalling and responses
    journal, October 2013


    Stalking intermediates in oxygen activation by iron enzymes: Motivation and method
    journal, April 2006


    Enlist E3™ Soybean Sensitivity and Enlist™ Herbicide-Based Program Control of Sumatran Fleabane ( Conyza sumatrensis )
    journal, June 2018

    • Frene, Rafael L.; Simpson, David M.; Buchanan, Marcos Baez
    • Weed Technology, Vol. 32, Issue 4
    • DOI: 10.1017/wet.2018.29

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    journal, August 1996


    Substrate-Triggered Formation and Remarkable Stability of the C−H Bond-Cleaving Chloroferryl Intermediate in the Aliphatic Halogenase, SyrB2
    journal, May 2009

    • Matthews, Megan L.; Krest, Courtney M.; Barr, Eric W.
    • Biochemistry, Vol. 48, Issue 20
    • DOI: 10.1021/bi900109z

    Evolution in Action: Plants Resistant to Herbicides
    journal, June 2010


    Role of the jelly-roll fold in substrate binding by 2-oxoglutarate oxygenases
    journal, December 2012

    • Aik, WeiShen; McDonough, Michael A.; Thalhammer, Armin
    • Current Opinion in Structural Biology, Vol. 22, Issue 6
    • DOI: 10.1016/j.sbi.2012.10.001

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    • Gerlt, John A.; Bouvier, Jason T.; Davidson, Daniel B.
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    • Terwilliger, Thomas C.; DiMaio, Frank; Read, Randy J.
    • Journal of Structural and Functional Genomics, Vol. 13, Issue 2
    • DOI: 10.1007/s10969-012-9129-3

    Structural basis for the enantiospecificities of R - and S- specific phenoxypropionate/α-ketoglutarate dioxygenases
    journal, June 2006

    • Müller, Tina A.; Zavodszky, Maria I.; Feig, Michael
    • Protein Science, Vol. 15, Issue 6
    • DOI: 10.1110/ps.052059406

    Manipulation and Sensing of Auxin Metabolism, Transport and Signaling
    journal, April 2018

    • Fukui, Kosuke; Hayashi, Ken-ichiro
    • Plant and Cell Physiology, Vol. 59, Issue 8
    • DOI: 10.1093/pcp/pcy076

    Weed resistance to synthetic auxin herbicides: Weed resistance to synthetic auxin herbicides
    journal, February 2018

    • Busi, Roberto; Goggin, Danica E.; Heap, Ian M.
    • Pest Management Science, Vol. 74, Issue 10
    • DOI: 10.1002/ps.4823